Further records of the deep-sea pandalid shrimp Heterocarpus chani Li, 2006 (Crustacea, Decapoda, Caridea) from southern India

Abstract The commercial deep-sea caridean shrimp Heterocarpus gibbosus Spence Bate, 1888 has long been recorded from India and constitutes an important part of the catches in the context of the further development of deep-sea fisheries in India. A recent survey in some deep-sea fishing ports in southern India, however, revealed that all material previously reported as “H. gibbosus” is actually a misidentification of its closely related species H. chani Li, 2006, which has only recently been reported from India. More detailed comparisons allowed the discovery of more distinctive characters between H. chani and H. gibbosus.


Introduction
The commercial deep-sea caridean shrimp Heterocarpus gibbosus Spence Bate,1888 was thought to be widely distributed in the Indo-West Pacific (Chace 1985, Crosnier 1988 and in some areas as being rather abundant (Holthuis 1980, Chan andYu 1987). Recently, however, this species was split into four species (Li 2006, Yang et al. 2010) mainly based on the height of the rostral crest, the development of the boss on the third abdominal somite and the length of the exopod of the third maxilliped. Specimens previously referred to this species from the western Pacific are not the true H. gibbosus but are instead H. abulbus Chu, 2010 andH. corona Yang, Chan &Chu, 2010. These two western Pacific species are rather different from H. gibbosus in having either a much lower or higher rostral crest (the low crest species, H. abulbus also has an indistinct abdominal boss). The other recently described species, H. chani Li, 2006, is very similar to H. gibbosus but with a much shorter exopod of the third maxilliped (Li 2006, Yang et al. 2010 and is currently mainly known from the South China Sea and the Philippines (Li and Chan 2013) as well as a short report from India (Kuberan et al. 2015). Other than co-occurring together with H. chani in the South China Sea and the Philippines, H. gibbosus is presumed to be the main species of this species complex in the Indian Ocean.
Heterocarpus gibbosus has long been reported from India (e.g., Wood-Mason and Alcock 1892, Alcock 1901, Kemp and Swell 1912, George and Rao 1967, Suseelan 1976, Radhakrishnan et al. 2012, Samuel et al. 2016, see also synonymy list in Fransen 2006) and now forms a major part of the catch in the deep-sea fisheries of India (e.g., Rajan et al. 2001, Kurup et al. 2008, Radhika Rajasree and Madhusoodana Kurup 2011, Rajool Shanis et al. 2012, 2014. However, recently a brief local technical report recorded H. chani from southern India (Kuberan et al. 2015). A visit of the third author (TYC) to the deep-sea fishing ports in southern India also found that the abundant materials identified there as "H. gibbosus" are actually all H. chani. The present work reports this finding. Detailed comparisons of these two species also revealed more differences between them. The material examined is deposited in the Department of Aquatic Biology and Fisheries, University of Kerala (DABFUK), National Taiwan Ocean University (NTOU), Lee Kong Chian Natural History Museum, Singapore (ZRC) and Oxford University Museum of Natural History (OUMNH). Additional materials for comparisons are those reported from the Philippines in Li and Chan (2013) and deposited in NTOU, with 69 specimens of H. gibbosus and 66 specimens of H. chani. Size measurements given are carapace length (cl) measured dorsally from the postorbital margin to the posterior margin of the carapace. Partial sequences of mitochondrial cytochrome c oxidase I (COI) gene data were generated by following the methods outlined in Yang et al. (2010).  Diagnosis. Rostrum far overreaching scaphocerite, 0.6-1.0 times as long as carapace. Rostrum dorsally armed with 7-10 teeth including 4-5 teeth on carapace posterior to orbital margin, ventrally armed with 10-16 teeth along entire length but with distal 2-3 teeth obscure. Rostral crest moderately elevated. Two lateral carinae on carapace, postorbital carina extending posteriorly almost to posterior margin of carapace and distinctly recurved downwards at posterior end. Branchiostegal carina sharp and extending posteriorly to 75-80% of carapace length ( Figs. 2A-B). Abdominal tergites without spine, boss on third somite distinct and with lateral borders somewhat carinate, width 0.2-0.3 and length 0.7-0.8 times as long as somite (Fig. 3C); only pleura IV and V bearing posteroventral tooth. Telson bearing 4 pairs of dorsolateral and 3 pairs of distal spines. Maxilliped III with exopod very short, 0.2-0.3 times as long as antepenultimate segment (Fig. 2C). Pereiopod III with carpus and ischium bearing 0-2 spines, merus with 1-6 mesial and 10-15 lateral spines, dactylus 0.2-0.4 times as long as propodus. Pereiopod IV with carpus bearing 1-2 spines, merus with 1 distinct apical spine and 10-13 lateral spines, ischium with 2 spines. Pereiopod V with carpus bearing 0-1 spines, merus with 10-13 lateral spines, ischium without any spine (Fig. 2D-F).

Heterocarpus chani Li, 2006
Coloration. Body generally orange red to rose red, rostrum whitish in anterior half but with tip often reddish. Eyes dark brown. Basal parts of antennular and antennal flagella whitish (more so in former). Scaphocerite with distal part whitish. Ventral lateral carina of carapace sometimes whitish except at tip (i.e. branchiostegal spine). Posterior border of carapace and anterior margin of abdominal somite I whitish. Maxilliped III with penultimate segment and sometimes also distal part of antepenultimate segment whitish. Pereiopod I with posterior part of carpus and sometimes also anterior part of merus whitish. Longer pereiopod II with chela, carpus and anterior part of merus whitish. Shorter pereiopod II only with basal carpus and distal merus whitish. Pereiopods III with propodus, carpus and anterior 1/2-1/3 of merus whitish. Pereiopods IV and V with propodus, carpus, merus and sometimes even entire pereiopod whitish except for reddish dactylus. Eggs greenish brown.
Distribution. Only known with certainty from the South China Sea, Philippines and southern India, at depths of 382 (perhaps as shallow as 200 m, see Kuberan et al. 2015) to 888 m.

Remarks.
Although Heterocarpus gibbosus Spence Bate, 1888 (type locality: Bohol Sea, The Philippines, see Li et al. 2007, Anonymous 2009) has long been reported from India, going back to soon after the original description of the species (Wood-Mason and Alcock 1892). Although recently considered as an important catch in the local deep-sea fishery (e.g., Rajan et al. 2001, Kurup et al. 2008, Rajasree and Kurup 2011, Rajool Shanis et al. 2012, 2014, the abundant specimens observed in three deep-sea fishing ports in southern India (Sakthikulangara, Muttom and Tuticorin, only specimens kept as vouchers were listed in Material examined) all actually represent H. chani without exception. Thus, the brief record of H. chani in India by Kurberan et al. (2015) is confirmed. The southern Indian material of H. chani agrees well with that reported from the South China Sea and the Philippines (Li 2006, Li andChan 2013). The only observed difference is the length of the rostrum being more frequently shorter in the Indian population. About half of the Indian specimens have the rostrum 0.6-0.7 times as long as the carapace in contrast to only about 1/10 of the comparative Philippines material with a shorter rostrum. Comparison of the COI sequences (657 bps) between the short (GenBank accession nos. MF149971-MF149973) and long rostral (MF149974) forms in the Indian material shows only 0.2-0.6% divergence, while genetic divergences between the Indian and Philippine materials (GQ302748, GQ302750, GQ302752, GQ302754) are 2.1-2.7 %. COI sequence divergences of less than 3% are generally considered to be intraspecific in decapod crustaceans (e.g.  Darling 2011, Vergamini et al. 2011, Yang et al. 2016. The coloration of the Indian material also generally agrees with that from the Philippines (Fig. 1, Li 2006: fig. 4, Yang et al. 2010: fig.5E, Li and Chan 2013 fig. 1B).
While H. chani exhibits a high genetic divergence from H. gibbosus (GQ302740, GQ302742, GQ302744, GQ302746, with 10.0-11.5% COI sequence divergence, also see Yang et al. 2010), the two species are morphologically very similar and mainly differ in the relative length of the exopod on the third maxilliped (Li 2006). More careful comparison of the present material reveals that there are three more, somewhat, subtle differences between these two species. The posterior end of the postorbital carina is distinctly ridged and recurved downwards in H. chani (Fig. 3A), but becomes rather indistinct and not bending downwards in H. gibbosus (Fig. 3B). The abdominal boss is more distinct and with the lateral borders ridged in H. chani (Fig. 3C) whilst in H. gibbosus, the abdominal boss is relatively less distinct and with the lateral borders not forming ridges (Fig. 3D). The posterior pereiopods each have a distinct red band on the anterior part of the merus in H. gibbosus (Li 2006  Although more differences are now enumerated between H. chani and H. gibbosus, it still cannot be deduced if the numerous reports of H. gibbosus from India in reality refer to that species or indeed solely represent H. chani, because all these records are too brief or did not list nor discuss any of the above distinctive characters. However, the "H. gibbosus" specimens from SW Cochin reported by George and Rao (1967) were described as having an abdominal boss with rather prominent median carination, and therefore likely represent H. chani instead. The "Heterocarpus ? gibbosus" illustrated by Wood-Mason and Alcock (1892: fig. 6), though lacking an abdominal boss, likely also represents H. chani since it has a shorter rostrum and with the posterior end of the postorbital carina sloping downwards. The rough line-drawing of "Heterocarpus gibbosus" provided in Suseelan (1974: fig. 2) also shows a posteriorly recurved downward postorbital carina. Thus, whether H. gibbosus truly occurs in India continues to be in need of confirmation.